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Originally, these were basilicas under the direction of a permanently appointed presbyter and corresponding to what would now be called parish churches. They were known as tituli or tituli presbyterales, distinguished from one another by the name of the founder or proprietor who held the property in custody for the Church.[4] For instance, the Titulus Aemilianae, now the church of the Santi Quattro Coronati, drew its name from its foundress, who doubtless owned the extensive suburban Roman villa whose foundations remain under the church and whose audience hall became the ecclesiastical basilica. The most ancient reference to such a Roman church is in the Apology against the Arians of Athanasius[4] in the fourth century, which speaks of a council of bishops assembled "in the place where the Presbyter Vito held his congregation".[5]

By the end of the 5th century they numbered 25, as is confirmed by the Liber Pontificalis. The same number, though with different identities, is given in the reports of councils held in Rome in 499 and 595. In 1120, the number is given as 28.[4] Many more have received the status of titular churches in modern times.

In 1059, the right of electing the pope was reserved to the bishops of the seven suburbicarian sees, the priests in charge of the titular churches and the clergy in charge of the deaconries. These were known collectively as the cardinals.

Accordingly, as ecclesiastics from outside Rome came to be appointed cardinals, they were assigned theoretical responsibility for certain Roman parish churches, a legal fiction establishing their position within the Pope's diocese, the see of Rome. They had no obligation to reside in Rome and so were not personally responsible for the pastoral care of the titular churches assigned to them, a practice still in force today.

Today, the cardinal priests have a loose patronal relationship with their titular churches. Their names and coats of arms are inscribed on plaques in the churches, they are expected to preach at the church occasionally when they are in Rome, and many raise funds for their church's maintenance and restoration, but they no longer participate in the actual management of the churches. There are now 143 presbyteral titular churches. Likewise, the cardinal bishops are given only honorary title to the 7 suburbicarian dioceses, and the cardinal deacons are given a similar relationship to the churches of their 69 deaconries.

The patriarchs of the Eastern Catholic Churches who become cardinals constitute an exception: their own patriarchal see is counted as their title.[6] They belong to the order of cardinal bishops and, in the order of precedence, come before the cardinal priests and immediately after the cardinals who hold the titles of the seven suburbicarian sees.

The term "titular church" is sometimes loosely applied to the deaconries diaconiae assigned to the cardinal deacons. Originally, they were charitable institutions first mentioned in connection with Pope Benedict II (684–685). Pope Adrian I (772–795) fixed their number at 18, a number that remained constant until the 16th century.[4]